The Association Between the Low Muscle Mass and Osteoporosis in Elderly Korean People

ORIGINAL ARTICLE Musculoskeletal Disorders http://dx.doi.org/10.3346/jkms.2014.29.7.995 • J Korean Med Sci 2014; 29: 995-1000

The Association between the Low Muscle Mass and Osteoporosis in Elderly Korean People

Sunyoung Kim,1,2 Chang Won Won,1 The purpose of this study was to predict osteoporosis risk as decreasing muscle mass and to Byung Sung Kim,1 Hyun Rim Choi,1 declare the cut-off value of low muscle mass in an elderly Korean population. This study and Min Young Moon1 was based on data from the 2008-2010 Korea National Health and Nutritional Examination Surveys (KNHANES). The subjects included 1,308 men and 1,171 women over 65 yr. Bone 1Department of Family Medicine, College of Medicine, Kyung Hee University, Seoul; 2Department mineral density (BMD) and appendicular skeletal muscle (ASM) were measured by dual of Medicine, Graduate School Ewha Womans energy X-ray absorptiometry (DXA), and appendicular skeletal muscle was adjusted by University, Seoul, Korea height as a marker of sarcopenia. After confirming the correlation between low muscle mass and BMD, the best cut-off value of muscle mass to estimate osteoporosis was Received: 23 December 2013 Accepted: 24 April 2014 suggested through the receiver operating characteristic (ROC) curve. For both men and women, BMD correlated positively with low muscle mass when ASM/Ht2 was used as a Address for Correspondence: marker for sarcopenia. The ROC curve showed that ASM/Ht2 was the best marker for Chang Won Won, MD osteoporosis at a cut-off value of 6.85 kg/m2 for men and 5.96 kg/m2 for women. When Department of Family Medicine, Kyung Hee University Hospital, 23 Kyunghee dae-ro, Dongdaemun-gu, Seoul 130-872, Korea these cut-off values were used to determine sarcopenia, the risk of osteoporosis increased Tel: +82.2-958-8697, Fax: +82.2-958-8699 4.14 times in men and 1.88 times in women. In particular, men (OR 2.12) with sarcopenia E-mail: [email protected] were more greatly affected than women (OR 1.15), even after adjusting for osteoporosis Funding: There is no research grant or funding with respect to this manuscript. risk factors. In elderly Korean people, sarcopenia is positively correlated with BMD and there is a strong correlation between sarcopenia and osteoporosis with risk of bone fracture.

Keywords: Osteoporosis; Sarcopenia; Korea; KNHANES; Elderly Population

INTRODUCTION gartner et al. suggested defining sarcopenia based on appen dicular skeletal muscle divided by height squared (Ht2) (7). Jans According to the 2010 data from the Statistics Korea, the elderly sen et al. used biochemical impedance analysis (BIA) to mea population in Korea increased 24.3% from 2005 to 2010, which sure total muscle mass and divided this mass by weight to de was 12.2 times greater than the increase in the total population fine sarcopenia (4). In recent studies, sarcopenia is defined as a (2.0%) during the same time period (1, 2). With this significant systemic continuous decrease in skeletal muscle strength and increase in the elderly population, it is important that increas muscle mass so that the diagnosis of sarcopenia must be sup ing attention be given to help maintain their physical and social ported by decreased muscle mass and functional muscle strength functioning while minimizing chronic disease and disability to (8). Until now, many studies of muscle mass and BMD have enhance their quality of life. been carried out (9-11), and they showed that low muscle mass Decreased muscle mass and bone mineral density are signif is correlated with low BMD. Unfortunately, their study popula icant changes that occur with aging, and these are often associ tions were inconsistent and their definitions of sarcopenia dif ated with an inability to adapt to external stress resulting in falls, ferent. In our study, by presenting a cut-off value of the muscle trauma, functional disability, increased hospitalization, decreas loss that can predict osteoporosis in Korean elderly individuals, ed quality of life, and increased mortality (3-5). Thus, diagnos we attempted to identify the relationship between muscle loss ing osteoporosis and sarcopenia is not only important clinical and osteoporosis. ly, but also has significant public and social ramifications. De termining the relationship between osteoporosis and sarcope MATERIALS AND METHODS nia may help maintain musculoskeletal function and prevent fractures associated with accidental falls. Subjects The diagnostic criteria have already been established for os This study is based on data obtained in the second and third teoporosis (5), but there is still controversy regarding the diag years (2008-2009) of the Korea National Health and Nutritional nostic criteria and markers for sarcopenia. Early studies by Baum Examination Survey (KNHANES) IV and the first year (2010) of

© 2014 The Korean Academy of Medical Sciences. pISSN 1011-8934 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. eISSN 1598-6357 Kim S, et al. • Sarcopenia and Osteoporosis the KNHANES V (2). The KNHANES is a cross-sectional study samples were collected during the health examination survey. and has been conducted periodically since 1998 to assess the These samples, taken from the antecubital veins, were refriger health and nutritional status of the civilian non-institutional ated immediately and transported on dry ice to the designated ized population of Korea and has generated nationwide and central testing facility, and were analyzed within 24 hr of sam representative statistical data by self-administered question pling. Serum 25(OH)D levels were measured using a gamma naires on health status, health behaviors, and nutritional status. counter (1470 Wizard, Perkin-Elmer, Turku, Finland) with a ra Data was collected via household units and selected based on a dioimmunoassay (RIA) kit (DiaSorin, Stillwater, MN, USA) (2). stratified, multistage probability sampling design. The selection was made from sampling units based on the geographical area, Statistical analysis gender, and age using household registries. The details of the All data are presented as the mean ± standard error (SE) for the KNHANES IV and V have been previously described (12, 13). A continuous variables or as proportion (SE) for the categorical total of 4,772 individuals aged ≥ 65 yr participated. Of the 4,772 variables. The characteristics of the participants were compared participants, we excluded individuals who did not have DXA according to sex using independent sample Student’s t-tests for results (n = 1,452) and those with a history of stroke, coronary the continuous measures and Rao scatt chi-square tests for the artery disease, thyroid disease, lung disease, liver and renal dis categorical measures. Regression analysis was applied to assess ease, and any cancers and those taking medications likely to af the association between various parts of the BMDs and the two fect bone or soft tissue metabolism, such as thyroid hormone, indexes of low muscle mass. The receiver operating character bisphosphonates, SERM, or weight controlling drugs (n = 841). istic (ROC) curve analysis was performed to determine the best The exclusion criteria were aimed to ensure selection of healthy cut-off value of low muscle mass for indicating osteoporosis. participants and to minimize the confounding effects on mus The areas under the ROC curve (AUC) were investigated for os cle mass. The present study included 2,479 elderly participants teoporosis. The ROC curve was a graph of sensitivity plotted (1,308 men and 1,171 women). against (1-specificity) over all possible diagnostic cut-off values. The optimal cut-off values were obtained from the maximal Measurement of bone density and appendicular skeletal Youden’s index, calculated as (sensitivity+specificity-1) and the muscle mass best combination of sensitivity and specificity. The odds ratios All participants underwent the DXA (DISCOVERY-W fan-beam (ORs) and 95% confidence intervals (CIs) were calculated by densitometer; Hologic Inc., MA, USA) for assessment of BMD logistic analysis to confirm the impact of low muscle mass, which and body composition. Standardized daily quality control of was based on the cut-off value for osteoporosis, after making these DXA in instruments was performed using spine phantom adjustments for age, fat mass, calcium intake, vitamin D status, provided by the manufacturer before the study commenced. smoking, alcohol consumption, and physical activity. Statistical The BMD (g/cm2 or T-score) of the whole body, femoral neck, analyses were performed using the survey procedure of SAS and lumbar spine (L1-4) were analyzed. The diagnosis of osteo software (version 9.2; SAS Institute, Cary, NC, USA) to account porosis was made using the WHO T-score criteria (T-score < -2.5), for the complex sampling design and to provide nationally rep and the maximum BMD value for Japanese patients was used resentative prevalence estimates. P < 0.05 was considered sta as a reference due to the lack of established diagnostic criteria tistically significant. for Koreans (14, 15). Appendicular skeletal muscle (ASM) mass was calculated as the sum of muscle mass in arms and legs, as Ethics statement suming that all non-fat and non-bone tissue is skeletal muscle This study was approved by the institutional review board of (16). According to the definition proposed in previous studies, KyungHee University Hospital, in Seoul, Korea (approval ID: we used muscle mass indexes, the height adjusted ASM (ASM/ KMCIRB 1413-05). Informed consent was waived by the board. Ht2, kg/m2) (5, 7, 17). RESULTS Anthropometric and laboratory measurements Body weight and height were measured to the nearest 0.1 kg The study population comprised 1,308 men and 1,171 women and 0.1 cm, respectively. BMI was calculated as weight/height2 with an average age of 71.9 yr for men and 74.2 yr for women. (kg/m2). Waist circumference was measured at the midpoint Height, weight, waist circumference, and muscle index were between the lower border of the rib cage and the iliac crest us higher in men, and body fat index was higher in women. Dia ing a non-elastic tapeline. Blood pressure was measured twice betes was more prevalent in men, and hypertension and meta at a 5-min interval on the right arm using a standard mercury bolic syndrome were more prevalent in women (Table 1). Of sphygmomanometer (Baumanometer; Baum, Copiague, NY, the index for sarcopenia, ASM/Ht2 was positively correlated USA) and recorded as an average of the two readings. Blood with BMD in both men and women, and adjusting for age and

996 http://jkms.org http://dx.doi.org/10.3346/jkms.2014.29.7.995 Kim S, et al. • Sarcopenia and Osteoporosis

Table 1. General characteristics of Korean elderly population body fat, still resulted in a positive correlation (Table 2). Mean ± SD The ROC curve reflecting osteoporosis from ASM/Ht2 is shown 2 Parameters Men Women P value in Fig. 1. The AUC of ASM/Ht for the prediction of osteoporosis (n = 1,308) (n = 1,171) was 0.705 (95% CI, 0.679-0.730; P < 0.001) in men, and 0.598 Age (yr) 71.9 ± 0.2 74.2 ± 0.2 < 0.001 (95% CI, 0.569-0.627; P < 0.001) in women. The best cut-off val Weight (kg) 62.8 ± 0.3 54.1 ± 0.3 < 0.001 ue of ASM/Ht2 for indicating osteoporosis, according to the max Height (cm) 164.8 ± 0.2 150 ± 0.2 < 0.001 2 Body mass index (kg/m2) 23.1 ± 0.1 24 ± 0.1 < 0.001 imum of the Youden index, was 6.85 kg/m in men and 5.96 kg/ Waist circumference (cm) 84.5 ± 0.3 83.1 ± 0.3 0.004 m2 in women. Sensitivity and specificity were 66.9% and 66% in ASM/Weight 31 ± 0.1 24.7 ± 0.1 < 0.001 men, and 62% and 53.5% in women, respectively. ASM/Height2 (kg/m2) 7.1 ± 0 5.9 ± 0.07 < 0.001 Total femur BMD (g/cm2) 0.878 ± 0.004 0.687 ± 0.004 < 0.001 Odds ratios (ORs) for the low muscle mass in relation to os Femoral neck BMD (g/cm2) 0.7 ± 0.004 0.542 ± 0.003 < 0.001 teoporosis are presented in Table 3. Both men and women sub 2 Lumbar spine BMD (g/cm ) 0.928 ± 0.005 0.732 ± 0.005 < 0.001 jects in the lower muscle mass group had increased risk for os Whole body total BMD (g/cm2) 1.143 ± 0.005 0.942 ± 0.005 < 0.001 Total femur T-score -0.453 ± 0.032 -1.427 ± 0.034 < 0.001 teoporosis (men: OR, 4.14; 95% CI, 2.67-6.78; P < 0.001, women: Spine T-score -0.798 ± 0.044 -2.38 ± 0.042 < 0.001 OR, 1.88; 95% CI, 1.41-2.5; P < 0.001). After adjusting for osteo ± ± Femoral neck T-score -1.181 0.033 -2.442 0.031 < 0.001 porosis risk factors (age, fat mass, calcium intake, vitamin D sta Past history (%) Hypertension 56.5 (1.8) 66.6 (1.8) < 0.001 tus, smoking, alcohol consumption, and physical activity), this Diabetes mellitus 21.2 (1.2) 19.1 (1.6) 0.265 association remained statistically significant in men (men: OR, Metabolic syndrome* 41.2 (1.8) 63.1 (1.9) < 0.001 Drinking (%) < 0.001 2.21; 95% CI, 1.33-3.37; P = 0.0016, women: OR, 1.15; 95% CI, 0.81- Non to moderate drinker 33.4 (1.5) 71.7 (1.7) 1.65; P = 0.44) (Table 3). Heavy drinker† 66.6 (1.5) 28.9 (1.7) Smoking (%) < 0.001 Non or ex-smoker 72.8 (1.5) 92.6 (1.1) DISCUSSION Current smoker 27.2 (1.5) 7.4 (1.1) Exercise (%) < 0.001 In our study, using ASM/Ht2 as an index for sarcopenia, muscle No 78.0 (1.5) 84.7 (1.2) Moderate to severe‡ 22.0 (1.5) 15.2 (1.2) mass and BMD showed a positive correlation, verifying that as 25(OH)D (ng/mL) 18.4 ± 0.3 22.3 ± 0.4 < 0.001 muscle mass decreases, the BMD of each body part shows a Calcium intake (mg) 359.6 ± 21.7 482.0 ± 12.3 < 0.001 lower value as well. Especially through the ROC curve, ASM/ *Metabolic syndrome: three or more or the following five criteria were defined as hav- Ht2 well reflected the risk of osteoporosis and indicated the best ing metabolic syndrome 1) abdominal obesity by waist circumference cut off values 2 2 of ≥ 90 cm for men and ≥ 80 cm for women), 2) systolic blood pressure ≥ 130 cut-off values (men 6.85 kg/m , women 5.96 kg/m ) for sarco mmHg or diastolic blood pressure ≥ 85 mmHg or on antihypertensive medication, 3) penia. This result is similar to studies involving postmenopausal elevated fasting blood glucose (≥ 5.6 mM/L), 4) hypertriglyceridemia (≥ 1.7 mM/L), women and men concluding that there are correlations among and 5) low serum HDL cholesterol (< 1.3 mM/L in men and < 1.29 mM/L in women). †Heavy drinker was defined who drank more than 30 g/day; ‡Moderate exercise body weight, muscle mass, and osteoporosis (10, 18-20). It can was defined as strenuous physical activity performed for at least 20 min at a time at be explained that body weight acts as a stress on the skeletal least three times a week. SD, standard deviation; ASM, appendicular skeletal muscle; system to promote bone formation mechanically by stimulat BMD, bone mineral density.

Table 2. Association of sarcopenia index and bone mineral density, stratified by sex, age and fat mass Men Women Indexes β SE P β SE P Whole body BMD (g/cm2) ASM/Ht2 (kg/m2) 0.039† -0.005 < 0.001 0.023* -0.007 0.001 Model 1‡ 0.031† -0.005 < 0.001 0.016* -0.006 0.006 Model 2§ 0.026† -0.006 < 0.001 0.007 -0.006 0.24 Femur neck BMD (g/cm2) ASM/Ht2 (kg/m2) 0.055† -0.004 < 0.001 0.034† -0.005 < 0.001 Model 1 0.046† -0.005 < 0.001 0.025† -0.004 < 0.001 Model 2 0.039† -0.005 < 0.001 0.016† -0.004 < 0.001 Femur total BMD (g/cm2) ASM/Ht2 (kg/m2) 0.067† -0.005 < 0.001 0.047† -0.005 < 0.001 Model 1 0.059† -0.005 < 0.001 0.036† -0.004 < 0.001 Model 2 0.051† -0.005 < 0.001 0.027† -0.005 < 0.001 L-Spine BMD (g/cm2) ASM/Ht2 (kg/m2) 0.061† -0.006 < 0.001 0.034† -0.007 < 0.001 Model 1 0.06† -0.007 < 0.001 0.028† -0.006 < 0.001 Model 2 0.042† -0.006 < 0.001 0.005 -0.006 0.48 *P < 0.05; †P < 0.001; ‡Model 1: adjusted for age; §Model 2: adjusted for age and fat mass. BMD, bone mineral density; ASM, appendicular skeletal muscle; Ht, height; Wt, weight. http://dx.doi.org/10.3346/jkms.2014.29.7.995 http://jkms.org 997 Kim S, et al. • Sarcopenia and Osteoporosis

Men Women 1.00 1.00 ASM/Ht2 < 6.85 kg/m2 ASM/Ht2 < 5.96 kg/m2

0.75 0.75

0.50 0.50 Sensitivity Sensitivity

0.25 0.25

0.00 0.00 0.00 0.25 0.50 0.75 1.00 0.00 0.25 0.50 0.75 1.00 1-Specificity A 1-Specificity B

Fig. 1. Receiver operating characteristic (ROC) curve of sarcopenia reflecting osteoporosis in Korean Elderly. The cut-off value of ASM/Ht2 was (A) 6.85 kg/m2 in men (area under the curve = 0.705; 95% CI, 0.679-0.730; P < 0.001 sensitivity 66.9%, specificity 66%), B( ) 5.96 kg/m2 in women (area under the curve = 0.598; 95% CI, 0.569-0.627; P < 0.001 sensitivity 62%, specificity 53.5%).

Table 3. Odds ratios (OR) and 95% confidence intervals (CI) for osteoporosis accord- sarcopenia (men 6.3%, women 4.1%) compared to Western coun ing to cutoff value of sarcopenia index in Korean Elderly tries when using ASM/Ht2 as the sarcopenia index (cut-off val Osteoporosis* ues for men and women were 7.40 kg/m2 and 5.14 kg/m2, re Sarcopenia index OR (95% CI) P value spectively). In a KLoSHA study with a sample population of Men adults older than 65 yr, the prevalence of sarcopenia was 35.3% ASM/Ht2 (kg/m2) < 6.85 4.14¶ (2.67-6.78) < 0.001 in men and 13.4% in women when ASM/Ht2 was used as the Model 1† 3.85¶ (2.34-5.47) < 0.001 Model 2‡ 2.63¶ (1.73-4) < 0.001 sarcopenia index (cut-off values for men and women were 7.09 Model 3§ 2.12ll (1.33-3.37) 0.0016 kg/m2 and 5.27 kg/m2, respectively) (17). But a study of the prev Women alence of sarcopenia in Korea using the KNHANES data showed ASM/Ht2 (kg/m2) < 5.96 1.88¶ (1.41-2.5) < 0.001 Model 1† 1.77¶ (1.3-2.39) < 0.001 that weight-adjusted ASM is better than height-adjusted ASM Model 2‡ 1.31 (0.96-1.79) 0.08 in defining sarcopenia. When using ASM/Ht2, the prevalence of Model 3§ 1.15 (0.81-1.65) 0.44 sarcopenia was 12.4% in men and 0.1% in women (cut-off val *Osteoporosis: T-score ≤ -2.5 at femoral neck, total or lumbar spine; †Model 1: ad- ues for men and women were 6.58 kg/m2 and 4.59 kg/m2, re justed for age; ‡Model 2: adjusted for age and fat mass; §Model 3: adjusted for age, fat mass, calcium intake, vitamin D status, smoking, alcohol consumption, physical spectively) (12). Though these studies performed in Korea seem activity; llP < 0.05; ¶P < 0.001. ASM, appendicular skeletal muscle. to suggest different cut-off values, this is because each study en rolled different study populations including various group of ages. ing osteocytes to increase bone density (21), and muscle mass, The present study, similar to other Korean studies, found that like fat mass may have a protective effect on bone density through ASM/Ht2 was the best sarcopenia index for indicating osteopo hormones (22). Also, the association between greater muscle rosis, with cut-off values at 6.85 kg/m2 in men and 5.96 kg/m2 in mass and greater bone density is likely to be determined by mul women. The cut-off value for men ranged between Sarcopenia tiple factors including common nutrition, life style and genes I (7.50) and II (6.58), and the cut-off value in women was higher regulating size (23-24). than Sarcopenia I (5.38), which was the standard in previous Many studies have focused on sarcopenia since Irwin Rosen Korean studies (12). The prevalence of sarcopenia in this study berg first identified the condition in 1989 (25) but a precise defi was 39.5% in men and 58.1% in women. Previous studies were nition, measurement method, and index of sarcopenia have yet limited in that the cut-off value for women was too low to deter to be established. Baumgartner et al. measured ASM with DXA mine prevalence, but using ASM/Ht2 as an index seems to have and defined sarcopenia as less than- 2 standard deviations from addressed this issue. In addition, when sarcopenia was based the mean of ASM/Ht2 in a young population (7). on the optimal cut-off value, the sarcopenia group had increased In Korea, interest in sarcopenia has increased, and numer risk of osteoporosis both in men (OR, 4.14; P < 0.001) and wom ous studies have been carried out. Kim et al.(26) studied sarco en (OR, 1.88; P < 0.001). In particular, men (OR, 2.12; P = 0.0016) penia in a Korean population and found a lower prevalence of with sarcopenia were more greatly affected than women (OR,

998 http://jkms.org http://dx.doi.org/10.3346/jkms.2014.29.7.995 Kim S, et al. • Sarcopenia and Osteoporosis

1.15; P = 0.44), even after adjusting for age, fat mass, calcium may help prevent accidental falls and bone fractures. intake, vitamin D status, smoking, alcohol consumption, and physical activity. This was demonstrated in previous studies ACKNOWLEDGMENT showing that bone mass in men was more closely related to muscle mass than in women (27-31). The gender difference in The authors wish to acknowledge the statistical support of KD the relationship between bone and muscle are explained by Han. gender specific effects of sex hormones. In men, changes to bone and muscle are controlled by increasing levels of testosterone DISCLOSURE and IGF-1 resulting in increased muscle mass and strength, whe reas in women, the higher level of estrogen results in bone mass The authors have no conflicts of interest to disclose. tending to increase more rapidly in relation to muscle (27, 29). And in both genders, aging causes loss in bone and muscle; ORCID and the bone and muscle relationship is affected by gender dif ferences in the rate of bone and muscle loss (32). Especially, Sunyoung Kim http://orcid.org/0000-0003-4115-4455 age-related decrease in testosterone and IGF-1 levels may lead Chang Won Won http://orcid.org/0000-0002-6429-4461 to decrease in muscle and bone in men, while, absolute level Byung Sung Kim http://orcid.org/0000-0002-4984-6918 and degree of decline in testosterone are much lower in wom Hyun Rim Choi http://orcid.org/0000-0003-4356-2831 en, muscle mass can be relatively preserved. In addition, me Min Young Moon http://orcid.org/0000-0002-7207-8155 chanical strain and estrogen share a common pathway involv ing activation of estrogen receptor-α (ER-α), and a decline in REFERENCES ER-α with menopause reduces the ability of mechanical load ing to induce an osteogenic response (33-35). This mechano 1. Statistics Korea. 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